Aromatase, aromatase inhibitors, and breast cancer

Journal of Steroid Biochemistry and Molecular Biology

Volumn 125, Issue 1-2, 2011, Pages 13-22

  Chumsri, Saranya ^a   Howes, Timothy ^a   Bao, Ting ^a   Sabnis, Gauri ^a   Brodie, Angela ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Aromatase inhibitors; Breast cancer

Indexed keywords

AMINOGLUTETHIMIDE; ANASTROZOLE; AROMATASE; AROMATASE INHIBITOR; ESTROGEN RECEPTOR; EXEMESTANE; FADROZOLE; FORMESTANE; GROWTH FACTOR RECEPTOR; LETROZOLE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PYRIDOGLUTETHIMIDE; TAMOXIFEN; VOROZOLE; ZOLEDRONIC ACID;

BREAST CANCER; CANCER PATIENT; CANCER RELAPSE; CANCER RESEARCH; CHEMOPROPHYLAXIS; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; DRUG TOLERABILITY; FRACTURE; HEADACHE; HOT FLUSH; HUMAN; INNATE IMMUNITY; METASTASIS; MUSCULOSKELETAL DISEASE; NONHUMAN; OSTEOPENIA; OSTEOPOROSIS; REVIEW; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT; VAGINAL DRYNESS;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; AROMATASE; AROMATASE INHIBITORS; BREAST NEOPLASMS; ESTROGENS; FEMALE; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 79957698092     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.02.001     Document Type: Review

References (110)

1. D.P. McDonnell, and J.D. Norris Connections and regulation of the human estrogen receptor Science 296 5573 2002 1642 1644 (Pubitemid 34579150)
2. G.G. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.A. Gustafsson Cloning of a novel receptor expressed in rat prostate and ovary Proc. Natl. Acad. Sci. U.S.A. 93 12 1996 5925 5930 (Pubitemid 26190778)
3. J.F. Couse, and K.S. Korach Estrogen receptor null mice: what have we learned and where will they lead us? Endocr. Rev. 20 3 1999 358 417 (Pubitemid 30654784)
4. D.P. McDonnell The molecular pharmacology of SERMs Trends Endocrinol. Metab. 10 8 1999 301 311
5. E.A. Musgrove, and R.L. Sutherland Biological determinants of endocrine resistance in breast cancer Nat. Rev. Cancer 9 9 2009 631 643
6. G. Beatson On the treatment of inoperable cases of carcinoma of themamma. Suggestions for a new method of treatment with illustrative cases Lancet II 1896 104 107
7. R.R. Love, and J. Philips Oophorectomy for breast cancer: history revisited J. Natl. Cancer Inst. 94 19 2002 1433 1434 (Pubitemid 35243741)
8. V.C. Jordan, and A.M. Brodie Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer Steroids 72 1 2007 7 25 (Pubitemid 46037765)
9. B. Fisher, J.P. Costantino, C.K. Redmond, E.R. Fisher, D.L. Wickerham, and W.M. Cronin Endometrial cancer in tamoxifen-treated breast cancer patients: findings from the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14 J. Natl. Cancer Inst. 86 7 1994 527 537 (Pubitemid 24111008)
10. V.C. Jordan Tamoxifen: toxicities and drug resistance during the treatment and prevention of breast cancer Annu. Rev. Pharmacol. Toxicol. 35 1995 195 211
11. W.C. Schwarzel, W.G. Kruggel, and H.J. Brodie Studies on the mechanism of estrogen biosynthesis. 8. The development of inhibitors of the enzyme system in human placenta Endocrinology 92 3 1973 866 880
12. L.F. Macedo, G. Sabnis, and A. Brodie Aromatase inhibitors and breast cancer Ann. N. Y. Acad. Sci. 1155 2009 162 173
13. A.M. Brodie, W.C. Schwarzel, A.A. Shaikh, and H.J. Brodie The effect of an aromatase inhibitor 4-hydroxy-4-androstene-3,17-dione, on estrogen-dependent processes in reproduction and breast cancer Endocrinology 100 6 1977 1684 1695 (Pubitemid 8103835)
14. R.J. Santen, H. Brodie, E.R. Simpson, P.K. Siiteri, A. Brodie, History of aromatase: saga of an important biological mediator and therapeutic target, Endocr. Rev. 30(4) 343-375.
15. A.M. Brodie, W.M. Garrett, J.R. Hendrickson, C.H. Tsai-Morris, P.A. Marcotte, and C.H. Robinson Inactivation of aromatase in vitro by 4-hydroxy-4-androstene-3 17-dione and 4-acetoxy-4-androstene-3,17-dione and sustained effects in vivo Steroids 38 6 1981 693 702 (Pubitemid 12148995)
16. H.J. Burstein, A.A. Prestrud, J. Seidenfeld, H. Anderson, T.A. Buchholz, N.E. Davidson, K.E. Gelmon, S.H. Giordano, C.A. Hudis, J. Malin, E.P. Mamounas, D. Rowden, A.J. Solky, M.R. Sowers, V. Stearns, E.P. Winer, M.R. Somerfield, J.J. Griggs, American society of clinical oncology clinical practice guideline: update on adjuvant endocrine therapy for women with hormone receptor-positive breast cancer, J. Clin. Oncol.
17. E.A. Thompson Jr., and P.K. Siiteri Utilization of oxygen and reduced nicotinamide adenine dinucleotide phosphate by human placental microsomes during aromatization of androstenedione J. Biol. Chem. 249 17 1974 5364 5372
18. S.A. Chen, M.J. Besman, R.S. Sparkes, S. Zollman, I. Klisak, T. Mohandas, P.F. Hall, and J.E. Shively Human aromatase: cDNA cloning, Southern blot analysis, and assignment of the gene to chromosome 15 DNA 7 1 1988 27 38 (Pubitemid 18044631)
19. M. Akhtar, J.N. Wright, P. Lee-Robichaud, A review of mechanistic studies on aromatase (CYP19) and 17alpha-hydroxylase-17,20-lyase (CYP17), J. Steroid Biochem. Mol. Biol.
20. N. Harada Aberrant expression of aromatase in breast cancer tissues J. Steroid Biochem. Mol. Biol. 61 3-6 1997 175 184 (Pubitemid 27455676)
21. L.E. Valladares, and A.H. Payne Induction of testicular aromatization by luteinizing hormone in mature rats Endocrinology 105 2 1979 431 436 (Pubitemid 9241021)
22. 2O release from 1beta,2beta-3H-androgens J. Biol. Chem. 251 6 1976 1625 1631
23. C.R. Durham, H. Zhu, B.S. Masters, E.R. Simpson, and C.R. Mendelson Regulation of aromatase activity of rat granulosa cells: induction of synthesis of NADPH-cytochrome P-450 reductase by FSH and dibutyryl cyclic AMP Mol. Cell Endocrinol. 40 2-3 1985 211 219 (Pubitemid 15029676)
24. E.F. Hahn, S. Miyairi, and J. Fishman 19-Hydroxylation of androgens in the rat brain Proc. Natl. Acad. Sci. U.S.A. 82 9 1985 2728 2730 (Pubitemid 15096550)
25. E.R. Simpson, M.S. Mahendroo, G.D. Means, M.W. Kilgore, M.M. Hinshelwood, S. Graham-Lorence, B. Amarneh, Y. Ito, C.R. Fisher, and M.D. Michael Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis Endocr. Rev. 15 3 1994 342 355 (Pubitemid 24180792)
26. S. Sebastian, and S.E. Bulun A highly complex organization of the regulatory region of the human CYP19 (aromatase) gene revealed by the Human Genome Project J. Clin. Endocrinol. Metab. 86 10 2001 4600 4602 (Pubitemid 33020491)
27. B. Amarneh, C.J. Corbin, J.A. Peterson, E.R. Simpson, and S. Graham-Lorence Functional domains of human aromatase cytochrome P450 characterized by linear alignment and site-directed mutagenesis Mol. Endocrinol. 7 12 1993 1617 1624 (Pubitemid 24034244)
28. J.T. Kellis Jr., and L.E. Vickery Purification and characterization of human placental aromatase cytochrome P-450 J. Biol. Chem. 262 9 1987 4413 4420 (Pubitemid 17102645)
29. E.D. Lephart, K.G. Peterson, J.F. Noble, F.W. George, and M.J. McPhaul The structure of cDNA clones encoding the aromatase P-450 isolated from a rat Leydig cell tumor line demonstrates differential processing of aromatase mRNA in rat ovary and a neoplastic cell line Mol. Cell Endocrinol. 70 1 1990 31 40 (Pubitemid 20097821)
30. S. Karkola, H.D. Holtje, and K. Wahala A three-dimensional model of CYP19 aromatase for structure-based drug design J. Steroid Biochem. Mol. Biol. 105 1-5 2007 63 70 (Pubitemid 47211957)
31. Y.C. Kao, L.L. Cam, C.A. Laughton, D. Zhou, and S. Chen Binding characteristics of seven inhibitors of human aromatase: a site-directed mutagenesis study Cancer Res. 56 15 1996 3451 3460 (Pubitemid 26251636)
32. J. Fishman, H. Guzik, and D. Dixon Sterochemistry of estrogen biosynthesis Biochemistry 8 11 1969 4304 4309
33. D. Ghosh, J. Griswold, M. Erman, and W. Pangborn Structural basis for androgen specificity and oestrogen synthesis in human aromatase Nature 457 7226 2009 219 223
34. D. Ghosh, J. Griswold, M. Erman, W. Pangborn, X-ray structure of human aromatase reveals an androgen-specific active site, J. Steroid Biochem. Mol. Biol. 118(4-5) 197-202.
35. I.E. Smith, and M. Dowsett Aromatase inhibitors in breast cancer N. Engl. J. Med. 348 24 2003 2431 2442 (Pubitemid 36682823)
36. J. Geisler, B. Haynes, G. Anker, M. Dowsett, and P.E. Lonning Influence of letrozole and anastrozole on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, cross-over study J. Clin. Oncol. 20 3 2002 751 757 (Pubitemid 34111382)
37. J. Bonneterre, A. Buzdar, J.M. Nabholtz, J.F. Robertson, B. Thurlimann, M. von Euler, T. Sahmoud, A. Webster, and M. Steinberg Anastrozole is superior to tamoxifen as first-line therapy in hormone receptor positive advanced breast carcinoma Cancer 92 9 2001 2247 2258
38. J.M. Nabholtz, A. Buzdar, M. Pollak, W. Harwin, G. Burton, A. Mangalik, M. Steinberg, A. Webster, and M. von Euler Anastrozole is superior to tamoxifen as first-line therapy for advanced breast cancer in postmenopausal women: results of a North American multicenter randomized trial. Arimidex Study Group J. Clin. Oncol. 18 22 2000 3758 3767
39. H.T. Mouridsen Aromatase inhibitors in advanced breast cancer Semin. Oncol. 31 6 (Suppl. 12) 2004 3 8 (Pubitemid 40616918)
40. J. Bonneterre, B. Thurlimann, J.F. Robertson, M. Krzakowski, L. Mauriac, P. Koralewski, I. Vergote, A. Webster, M. Steinberg, and M. von Euler Anastrozole versus tamoxifen as first-line therapy for advanced breast cancer in 668 postmenopausal women: results of the Tamoxifen or Arimidex randomized group efficacy and tolerability study J. Clin. Oncol. 18 22 2000 3748 3757
41. H. Mouridsen, M. Gershanovich, Y. Sun, R. Perez-Carrion, C. Boni, A. Monnier, J. Apffelstaedt, R. Smith, H.P. Sleeboom, F. Janicke, A. Pluzanska, M. Dank, D. Becquart, P.P. Bapsy, E. Salminen, R. Snyder, M. Lassus, J.A. Verbeek, B. Staffler, H.A. Chaudri-Ross, and M. Dugan Superior efficacy of letrozole versus tamoxifen as first-line therapy for postmenopausal women with advanced breast cancer: results of a phase III study of the International Letrozole Breast Cancer Group J. Clin. Oncol. 19 10 2001 2596 2606 (Pubitemid 32451796)
42. T.P. Paridaens, and L. Dirix First line hormonal treatment for metastatic breast cancer with exemestane or tamoxifen in postmenopausal patients: a randomized phase III trial of the EORTC Breast Group Proc. Am. Soc. Clin. Oncol. 2004 6
43. A. Buzdar, J. Douma, N. Davidson, R. Elledge, M. Morgan, R. Smith, L. Porter, J. Nabholtz, X. Xiang, and C. Brady Phase III, multicenter, double-blind, randomized study of letrozole, an aromatase inhibitor, for advanced breast cancer versus megestrol acetate J. Clin. Oncol. 19 14 2001 3357 3366 (Pubitemid 32642188)
44. A. Buzdar, W. Jonat, A. Howell, S.E. Jones, C. Blomqvist, C.L. Vogel, W. Eiermann, J.M. Wolter, M. Azab, A. Webster, and P.V. Plourde Anastrozole: a potent and selective aromatase inhibitor, versus megestrol acetate in postmenopausal women with advanced breast cancer: results of overview analysis of two phase III trials. Arimidex Study Group J. Clin. Oncol. 14 7 1996 2000 2011 (Pubitemid 26230100)
45. P. Dombernowsky, I. Smith, G. Falkson, R. Leonard, L. Panasci, J. Bellmunt, W. Bezwoda, G. Gardin, A. Gudgeon, M. Morgan, A. Fornasiero, W. Hoffmann, J. Michel, T. Hatschek, T. Tjabbes, H.A. Chaudri, U. Hornberger, and P.F. Trunet Letrozole, a new oral aromatase inhibitor for advanced breast cancer: double-blind randomized trial showing a dose effect and improved efficacy and tolerability compared with megestrol acetate J. Clin. Oncol. 16 2 1998 453 461 (Pubitemid 28135586)
46. M. Kaufmann, E. Bajetta, L.Y. Dirix, L.E. Fein, S.E. Jones, N. Zilembo, J.L. Dugardyn, C. Nasurdi, R.G. Mennel, J. Cervek, C. Fowst, A. Polli, E. di Salle, A. Arkhipov, G. Piscitelli, L.L. Miller, and G. Massimini Exemestane is superior to megestrol acetate after tamoxifen failure in postmenopausal women with advanced breast cancer: results of a phase III randomized double-blind trial. The Exemestane Study Group J. Clin. Oncol. 18 7 2000 1399 1411 (Pubitemid 30205385)
47. P.E. Goss, E.P. Winer, I.F. Tannock, and L.H. Schwartz Randomized phase III trial comparing the new potent and selective third-generation aromatase inhibitor vorozole with megestrol acetate in postmenopausal advanced breast cancer patients. North American Vorozole Study Group J. Clin. Oncol. 17 1 1999 52 63 (Pubitemid 29022378)
48. J.F. Forbes, J. Cuzick, A. Buzdar, A. Howell, J.S. Tobias, and M. Baum Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial Lancet Oncol. 9 1 2008 45 53
49. B. Thurlimann, A. Keshaviah, A.S. Coates, H. Mouridsen, L. Mauriac, J.F. Forbes, R. Paridaens, M. Castiglione-Gertsch, R.D. Gelber, M. Rabaglio, I. Smith, A. Wardley, K.N. Price, and A. Goldhirsch A comparison of letrozole and tamoxifen in postmenopausal women with early breast cancer N. Engl. J. Med. 353 26 2005 2747 2757 (Pubitemid 43016814)
50. H. Mouridsen, A. Giobbie-Hurder, A. Goldhirsch, B. Thurlimann, R. Paridaens, I. Smith, L. Mauriac, J.F. Forbes, K.N. Price, M.M. Regan, R.D. Gelber, and A.S. Coates Letrozole therapy alone or in sequence with tamoxifen in women with breast cancer N. Engl. J. Med. 361 8 2009 766 776
51. M. Gnant, B. Mlineritsch, W. Schippinger, G. Luschin-Ebengreuth, S. Postlberger, C. Menzel, R. Jakesz, M. Seifert, M. Hubalek, V. Bjelic-Radisic, H. Samonigg, C. Tausch, H. Eidtmann, G. Steger, W. Kwasny, P. Dubsky, M. Fridrik, F. Fitzal, M. Stierer, E. Rucklinger, R. Greil, and C. Marth Endocrine therapy plus zoledronic acid in premenopausal breast cancer N. Engl. J. Med. 360 7 2009 679 691
52. N.U. Lin, and E.P. Winer Advances in adjuvant endocrine therapy for postmenopausal women J. Clin. Oncol. 26 5 2008 798 805 (Pubitemid 351264393)
53. R. Jakesz, M. Gnant, and R. Greil The benefits of sequencing adjuvant tamoxifen and anastrozole in postmenopausal women with hormone responsive early breast cancer: 5 year-analysis of ABCSG trial 8 The 28th Annual San Antonio Breast Cancer Symposium San Antonio, TX 2005
54. M. Kaufmann, W. Jonat, J. Hilfrich, H. Eidtmann, G. Gademann, I. Zuna, and G. von Minckwitz Improved overall survival in postmenopausal women with early breast cancer after anastrozole initiated after treatment with tamoxifen compared with continued tamoxifen: the ARNO 95 study J. Clin. Oncol. 25 19 2007 2664 2670 (Pubitemid 47123171)
55. F. Boccardo, A. Rubagotti, P. Guglielmini, A. Fini, G. Paladini, M. Mesiti, M. Rinaldini, S. Scali, M. Porpiglia, C. Benedetto, N. Restuccia, F. Buzzi, R. Franchi, B. Massidda, V. Distante, D. Amadori, and P. Sismondi Switching to anastrozole versus continued tamoxifen treatment of early breast cancer. Updated results of the Italian tamoxifen anastrozole (ITA) trial Ann. Oncol. 17 Suppl. 7 2006 10 14
56. R.C. Coombes, L.S. Kilburn, C.F. Snowdon, R. Paridaens, R.E. Coleman, S.E. Jones, J. Jassem, C.J. Van de Velde, T. Delozier, I. Alvarez, L. Del Mastro, O. Ortmann, K. Diedrich, A.S. Coates, E. Bajetta, S.B. Holmberg, D. Dodwell, E. Mickiewicz, J. Andersen, P.E. Lonning, G. Cocconi, J. Forbes, M. Castiglione, N. Stuart, A. Stewart, L.J. Fallowfield, G. Bertelli, E. Hall, R.G. Bogle, M. Carpentieri, E. Colajori, M. Subar, E. Ireland, and J.M. Bliss Survival and safety of exemestane versus tamoxifen after 2-3 years' tamoxifen treatment (Intergroup Exemestane study): a randomised controlled trial Lancet 369 9561 2007 559 570
57. D. Rea, A. Hasenburg, and C. Seynaeve Five years of exemestane as initial therapy compared to 5 years of tamoxifen followed by exemestane: The TEAM trial, a prospective, randomized, phase III trial in postmenopausal women with hormone-sensitive early breast cancer The 32nd Annual San Antonio Breast Cancer Symposium San Antonio, TX 2009
58. H.J. Stewart, R.J. Prescott, and A.P. Forrest Scottish adjuvant tamoxifen trial: a randomized study updated to 15 years J. Natl. Cancer Inst. 93 6 2001 456 462 (Pubitemid 32266538)
59. B. Fisher, J. Dignam, J. Bryant, and N. Wolmark Five versus more than five years of tamoxifen for lymph node-negative breast cancer: updated findings from the National Surgical Adjuvant Breast and Bowel Project B-14 randomized trial J. Natl. Cancer Inst. 93 9 2001 684 690 (Pubitemid 32492809)
60. R. Peto, and C. Davies ATLAS (Adjuvant Tamoxifen, Longer Against Shorter): international randomized trial of 10 versus 5 years of adjuvant tamoxifen among 11,500 women - preliminary results The 30th Annual San Antonio Breast Cancer Symposium San Antonio, TX 2007
61. R. Jakesz, R. Greil, M. Gnant, M. Schmid, W. Kwasny, E. Kubista, B. Mlineritsch, C. Tausch, M. Stierer, F. Hofbauer, K. Renner, C. Dadak, E. Rucklinger, and H. Samonigg Extended adjuvant therapy with anastrozole among postmenopausal breast cancer patients: results from the randomized Austrian Breast and Colorectal Cancer Study Group Trial 6a J. Natl. Cancer Inst. 99 24 2007 1845 1853 (Pubitemid 351767193)
62. P.E. Goss, J.N. Ingle, S. Martino, N.J. Robert, H.B. Muss, M.J. Piccart, M. Castiglione, D. Tu, L.E. Shepherd, K.I. Pritchard, R.B. Livingston, N.E. Davidson, L. Norton, E.A. Perez, J.S. Abrams, D.A. Cameron, M.J. Palmer, and J.L. Pater Efficacy of letrozole extended adjuvant therapy according to estrogen receptor and progesterone receptor status of the primary tumor: National Cancer Institute of Canada Clinical Trials Group MA.17 J. Clin. Oncol. 25 15 2007 2006 2011 (Pubitemid 46972784)
63. E.P. Mamounas, J.H. Jeong, D.L. Wickerham, R.E. Smith, P.A. Ganz, S.R. Land, A. Eisen, L. Fehrenbacher, W.B. Farrar, J.N. Atkins, E.R. Pajon, V.G. Vogel, J.F. Kroener, L.F. Hutchins, A. Robidoux, J.L. Hoehn, J.N. Ingle, C.E. Geyer Jr., J.P. Costantino, and N. Wolmark Benefit from exemestane as extended adjuvant therapy after 5 years of adjuvant tamoxifen: intention-to-treat analysis of the National Surgical Adjuvant Breast And Bowel Project B-33 trial J. Clin. Oncol. 26 12 2008 1965 1971
64. I.E. Smith, and L. Lipton Preoperative/neoadjuvant medical therapy for early breast cancer Lancet Oncol. 2 9 2001 561 570 (Pubitemid 33586869)
65. A.P. Forrest, P.A. Levack, U. Chetty, R.A. Hawkins, W.R. Miller, J.F. Smyth, and T.J. Anderson A human tumour model Lancet 2 8511 1986 840 842 (Pubitemid 17178039)
66. I.E. Smith, M. Dowsett, S.R. Ebbs, J.M. Dixon, A. Skene, J.U. Blohmer, S.E. Ashley, S. Francis, I. Boeddinghaus, and G. Walsh Neoadjuvant treatment of postmenopausal breast cancer with anastrozole, tamoxifen, or both in combination: the Immediate Preoperative Anastrozole, Tamoxifen, or Combined with Tamoxifen (IMPACT) multicenter double-blind randomized trial J. Clin. Oncol. 23 22 2005 5108 5116 (Pubitemid 46224019)
67. L. Cataliotti, A.U. Buzdar, S. Noguchi, J. Bines, Y. Takatsuka, K. Petrakova, P. Dube, and C.T. de Oliveira Comparison of anastrozole versus tamoxifen as preoperative therapy in postmenopausal women with hormone receptor-positive breast cancer: the Pre-Operative "Arimidex" compared to Tamoxifen (PROACT) trial Cancer 106 10 2006 2095 2103 (Pubitemid 43673229)
68. W. Eiermann, S. Paepke, J. Appfelstaedt, A. Llombart-Cussac, J. Eremin, J. Vinholes, L. Mauriac, M. Ellis, M. Lassus, H.A. Chaudri-Ross, M. Dugan, and M. Borgs Preoperative treatment of postmenopausal breast cancer patients with letrozole: a randomized double-blind multicenter study Ann. Oncol. 12 11 2001 1527 1532 (Pubitemid 34065880)
69. B. Thurlimann, R. Paridaens, D. Serin, J. Bonneterre, H. Roche, R. Murray, E. di Salle, S. Lanzalone, M.G. Zurlo, and G. Piscitelli Third-line hormonal treatment with exemestane in postmenopausal patients with advanced breast cancer progressing on aminoglutethimide: a phase II multicentre multinational study. Exemestane Study Group Eur. J. Cancer 33 11 1997 1767 1773 (Pubitemid 28129201)
70. P. Carlini, A. Frassoldati, S. De Marco, A. Casali, E.M. Ruggeri, M. Nardi, P. Papaldo, A. Fabi, F. Paoloni, and F. Cognetti Formestane, a steroidal aromatase inhibitor after failure of non-steroidal aromatase inhibitors (anastrozole and letrozole): is a clinical benefit still achievable? Ann. Oncol. 12 11 2001 1539 1543 (Pubitemid 34065882)
71. W.R. Miller, J. Bartlett, A.M. Brodie, R.W. Brueggemeier, E. di Salle, P.E. Lonning, A. Llombart, N. Maass, T. Maudelonde, H. Sasano, and P.E. Goss Aromatase inhibitors: are there differences between steroidal and nonsteroidal aromatase inhibitors and do they matter? Oncologist 13 8 2008 829 837
72. J. Geisler, D.C. Johannessen, G. Anker, and P.E. Lonning Treatment with formestane alone and in combination with aminoglutethimide in heavily pretreated breast cancer patients: clinical and endocrine effects Eur. J. Cancer 32A 5 1996 789 792
73. C. Harper-Wynne, J. English, L. Meyer, M. Bower, C. Archer, H.D. Sinnett, C. Lowdell, and R.C. Coombes Randomized trial to compare the efficacy and toxicity of cyclophosphamide, methotrexate and 5-fluorouracil (CMF) with methotrexate mitoxantrone (MM) in advanced carcinoma of the breast Br. J. Cancer 81 2 1999 316 322 (Pubitemid 29423712)
74. G. Bertelli, O. Garrone, M. Merlano, M. Occeli, L. Bertolotti, F. Castiglione, F. Pepi, O. Fusco, L. Del Mastro, and R.C. Leonard Sequential treatment with exemestane and non-steroidal aromatase inhibitors in advanced breast cancer Oncology 69 6 2005 471 477
75. N. Zilembo, E. Bajetta, E. Bichisao, A. Martinetti, I. La Torre, P. Bidoli, R. Longarini, T. Portale, E. Seregni, and E. Bombardieri The estrogen suppression after sequential treatment with formestane in advanced breast cancer patients Biomed. Pharmacother. 58 4 2004 255 259 (Pubitemid 38746753)
76. S. Chia, W. Gradishar, L. Mauriac, J. Bines, F. Amant, M. Federico, L. Fein, G. Romieu, A. Buzdar, J.F. Robertson, A. Brufsky, K. Possinger, P. Rennie, F. Sapunar, E. Lowe, and M. Piccart Double-blind, randomized placebo controlled trial of fulvestrant compared with exemestane after prior nonsteroidal aromatase inhibitor therapy in postmenopausal women with hormone receptor-positive, advanced breast cancer: results from EFECT J. Clin. Oncol. 26 10 2008 1664 1670
77. M.E. Hammond, D.F. Hayes, M. Dowsett, D.C. Allred, K.L. Hagerty, S. Badve, P.L. Fitzgibbons, G. Francis, N.S. Goldstein, M. Hayes, D.G. Hicks, S. Lester, R. Love, P.B. Mangu, L. McShane, K. Miller, C.K. Osborne, S. Paik, J. Perlmutter, A. Rhodes, H. Sasano, J.N. Schwartz, F.C. Sweep, S. Taube, E.E. Torlakovic, P. Valenstein, G. Viale, D. Visscher, T. Wheeler, R.B. Williams, J.L. Wittliff, A.C. Wolff, American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer, J. Clin. Oncol. 28(16) 2784-2795.
78. R.M. Elledge, S. Green, R. Pugh, D.C. Allred, G.M. Clark, J. Hill, P. Ravdin, S. Martino, and C.K. Osborne Estrogen receptor (ER) and progesterone receptor (PgR), by ligand-binding assay compared with ER, PgR and pS2, by immuno-histochemistry in predicting response to tamoxifen in metastatic breast cancer: a Southwest Oncology Group Study Int. J. Cancer 89 2 2000 111 117 (Pubitemid 30185917)
79. C.A. Lockwood, C. Ricciardelli, W.A. Raymond, R. Seshadri, K. McCaul, and D.J. Horsfall A simple index using video image analysis to predict disease outcome in primary breast cancer Int. J. Cancer 84 3 1999 203 208 (Pubitemid 29256742)
80. A.T. Ferguson, R.G. Lapidus, S.B. Baylin, and N.E. Davidson Demethylation of the estrogen receptor gene in estrogen receptor-negative breast cancer cells can reactivate estrogen receptor gene expression Cancer Res. 55 11 1995 2279 2283
81. Y.L. Ottaviano, J.P. Issa, F.F. Parl, H.S. Smith, S.B. Baylin, and N.E. Davidson Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells Cancer Res. 54 10 1994 2552 2555 (Pubitemid 24173735)
82. D. Sharma, N.K. Saxena, N.E. Davidson, and P.M. Vertino Restoration of tamoxifen sensitivity in estrogen receptor-negative breast cancer cells: tamoxifen-bound reactivated ER recruits distinctive corepressor complexes Cancer Res. 66 12 2006 6370 6378
83. X. Yang, A.T. Ferguson, S.J. Nass, D.L. Phillips, K.A. Butash, S.M. Wang, J.G. Herman, and N.E. Davidson Transcriptional activation of estrogen receptor alpha in human breast cancer cells by histone deacetylase inhibition Cancer Res. 60 24 2000 6890 6894 (Pubitemid 32059160)
84. X. Yang, D.L. Phillips, A.T. Ferguson, W.G. Nelson, J.G. Herman, and N.E. Davidson Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells Cancer Res. 61 19 2001 7025 7029 (Pubitemid 32946489)
85. G. Sabnis, L. Macedo, L. Gediya, V. Njar, and A. Brodie Upregulation of ERα and aromatase by HDACi MS-275 in an ER negative breast cancer xenograft model 90th Annual Meeting of Endocrine Society San Francisco, CA 2008 (abstract #P1-100)
86. G. Sabnis, O. Goloubeva, L. Macedo, L. Gediya, V. Njar, and A. Brodie Combination of HDACi entinostat (SNDX-275) with letrozole in provides superior control over tumor growth in MDA-MB-231 xenograft model The 31st Annual San Antonio Breast Cancer Symposium San Antonio, TX 2008
87. G. Sabnis, L. Gediya, V. Njar, and A. Brodie HDAC inhibitors sensitize ER negative breast cancer cells to AIs Breast Cancer Research and Treatment Proceedings of the 30th Annual San Antonio Breast Cancer Symposium San Antonio, TX 2007 (abstract # 2096)
88. L.F. Macedo, G. Sabnis, and A. Brodie Preclinical modeling of endocrine response and resistance: focus on aromatase inhibitors Cancer 112 Suppl. 3 2008 679 688 (Pubitemid 351186389)
89. D. Jelovac, G. Sabnis, B.J. Long, L. Macedo, O.G. Goloubeva, and A.M. Brodie Activation of mitogen-activated protein kinase in xenografts and cells during prolonged treatment with aromatase inhibitor letrozole Cancer Res. 65 12 2005 5380 5389 (Pubitemid 40834290)
90. R. Clarke, M.C. Liu, K.B. Bouker, Z. Gu, R.Y. Lee, Y. Zhu, T.C. Skaar, B. Gomez, K. O'Brien, Y. Wang, and L.A. Hilakivi-Clarke Antiestrogen resistance in breast cancer and the role of estrogen receptor signaling Oncogene 22 47 2003 7316 7339 (Pubitemid 37492898)
91. L. Shi, B. Dong, Z. Li, Y. Lu, T. Ouyang, J. Li, T. Wang, Z. Fan, T. Fan, B. Lin, Z. Wang, and Y. Xie Expression of ER-{alpha}36, a novel variant of estrogen receptor {alpha}, and resistance to tamoxifen treatment in breast cancer J. Clin. Oncol. 27 21 2009 3423 3429
92. R. Schiff, P. Reddy, M. Ahotupa, E. Coronado-Heinsohn, M. Grim, S.G. Hilsenbeck, R. Lawrence, S. Deneke, R. Herrera, G.C. Chamness, S.A. Fuqua, P.H. Brown, and C.K. Osborne Oxidative stress and AP-1 activity in tamoxifen-resistant breast tumors in vivo J. Natl. Cancer Inst. 92 23 2000 1926 1934 (Pubitemid 32036923)
93. Y. Zhou, C. Yau, J.W. Gray, K. Chew, S.H. Dairkee, D.H. Moore, U. Eppenberger, S. Eppenberger-Castori, and C.C. Benz Enhanced NF kappa B and AP-1 transcriptional activity associated with antiestrogen resistant breast cancer BMC Cancer 7 2007 59
94. A. Ring, and M. Dowsett Mechanisms of tamoxifen resistance Endocr. Relat. Cancer 11 4 2004 643 658 (Pubitemid 40065543)
95. G. Sabnis, O. Goloubeva, R. Gilani, L. Macedo, A. Brodie, Sensitivity to the aromatase inhibitor letrozole is prolonged after a "break" in treatment, Mol. Cancer Ther. 9(1) 46-56.
96. L.F. Macedo, G.J. Sabnis, O.G. Goloubeva, and A. Brodie Combination of anastrozole with fulvestrant in the intratumoral aromatase xenograft model Cancer Res. 68 9 2008 3516 3522
97. S. Kato, H. Endoh, Y. Masuhiro, T. Kitamoto, S. Uchiyama, H. Sasaki, S. Masushige, Y. Gotoh, E. Nishida, H. Kawashima, D. Metzger, and P. Chambon Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase Science 270 5241 1995 1491 1494
98. P.B. Joel, A.M. Traish, and D.A. Lannigan Estradiol-induced phosphorylation of serine 118 in the estrogen receptor is independent of p42/p44 mitogen-activated protein kinase J. Biol. Chem. 273 21 1998 13317 13323 (Pubitemid 28246906)
99. D. Chen, E. Washbrook, N. Sarwar, G.J. Bates, P.E. Pace, V. Thirunuvakkarasu, J. Taylor, R.J. Epstein, F.V. Fuller-Pace, J.M. Egly, R.C. Coombes, and S. Ali Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera Oncogene 21 32 2002 4921 4931
100. S.R. Johnston Enhancing the efficacy of hormonal agents with selected targeted agents Clin. Breast Cancer 9 Suppl. 1 2009 S28 S36
101. R.C. Wu, J. Qin, P. Yi, J. Wong, S.Y. Tsai, M.J. Tsai, and B.W. O'Malley Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic reponses to multiple cellular signaling pathways Mol. Cell 15 6 2004 937 949 (Pubitemid 39277990)
102. J. Font de Mora, and M. Brown AIB1 is a conduit for kinase-mediated growth factor signaling to the estrogen receptor Mol. Cell Biol. 20 14 2000 5041 5047 (Pubitemid 30431558)
103. G.J. Sabnis, L.F. Macedo, O. Goloubeva, A. Schayowitz, and A.M. Brodie Stopping treatment can reverse acquired resistance to letrozole Cancer Res. 68 12 2008 4518 4524
104. G. Sabnis, A. Schayowitz, O. Goloubeva, L. Macedo, and A. Brodie Trastuzumab reverses letrozole resistance and amplifies the sensitivity of breast cancer cells to estrogen Cancer Res. 69 4 2009 1416 1428
105. G. Sabnis, O. Goloubeva, D. Jelovac, A. Schayowitz, and A. Brodie Inhibition of the phosphatidylinositol 3-kinase/Akt pathway improves response of long-term estrogen-deprived breast cancer xenografts to antiestrogens Clin. Cancer Res. 13 9 2007 2751 2757 (Pubitemid 46788044)
106. A. Lipton, K. Leitzel, S.M. Ali, L. Demers, H.A. Harvey, H.A. Chaudri-Ross, D. Evans, R. Lang, W. Hackl, P. Hamer, and W. Carney Serum HER-2/neu conversion to positive at the time of disease progression in patients with breast carcinoma on hormone therapy Cancer 104 2 2005 257 263 (Pubitemid 40993251)
107. A. Lipton, S. Ali, and K. Leitzel HER-2 protein expression predicts response to trastuzumab in FISH-positive patients with metastatic breast cancer 31st AACR-CTRC San Antonio Breast Cancer Symposium San Antonio, TX 2008
108. P.K. Marcom, C. Isaacs, L. Harris, Z.W. Wong, A. Kommarreddy, N. Novielli, G. Mann, Y. Tao, and M.J. Ellis The combination of letrozole and trastuzumab as first or second-line biological therapy produces durable responses in a subset of HER2 positive and ER positive advanced breast cancers Breast Cancer Res. Treat. 102 1 2007 43 49 (Pubitemid 46294957)
109. J. Mackey, B. Kaufman, and M. Clemens Trastuzumab prolongs progression-free survival in hormone-dependent and HER2-positive metastatic breast cancer Breast Cancer Res. Treat. 100 Suppl. 1 2006 (abstract 3)
110. S. Johnston, J. Pippen Jr., X. Pivot, M. Lichinitser, S. Sadeghi, V. Dieras, H.L. Gomez, G. Romieu, A. Manikhas, M.J. Kennedy, M.F. Press, J. Maltzman, A. Florance, L. O'Rourke, C. Oliva, S. Stein, and M. Pegram Lapatinib combined with letrozole versus letrozole and placebo as first-line therapy for postmenopausal hormone receptor-positive metastatic breast cancer J. Clin. Oncol. 27 33 2009 5538 5546